Research Population genomic analysis of mango (Mangifera indica) suggests a complex history of domestication Emily J. Warschefsky1 and Eric J. B. von Wettberg1,2 1Biological Sciences, Florida International University, 11200 SW 8th St., Miami, FL 33199, USA; 2Plant and Soil Science, The University of Vermont, 63 Carrigan Drive, Burlington, VT, USA Summary Author for correspondence: Humans have domesticated diverse species from across the plant kingdom, yet much of our Emily J. Warschefsky foundational knowledge of domestication has come from studies investigating relatively few Tel: +1 604 827 3535 of the most important annual food crops. Here, we examine the impacts of domestication on Email: ewars001@fiu.edu genetic diversity in a tropical perennial fruit species, mango (Mangifera indica). Received: 1 September 2018 We used restriction site associated DNA sequencing to generate genomic single nucleotide Accepted: 21 January 2019 polymorphism (SNP) data from 106 mango cultivars from seven geographical regions along with 52 samples of closely related species and unidentified cultivars to identify centers of New Phytologist (2019) 222: 2023–2037 mango genetic diversity and examine how post-domestication dispersal shaped the geo- doi: 10.1111/nph.15731 graphical distribution of diversity. We identify two gene pools of cultivated mango, representing Indian and Southeast Asian Key words: domestication, Mangifera germplasm. We found no significant genetic bottleneck associated with the introduction of indica, perennial crop, population genomics, mango into new regions of the world. By contrast, we show that mango populations in intro- RADseq. duced regions have elevated levels of diversity. Our results suggest that mango has a more complex history of domestication than previ- ously supposed, perhaps including multiple domestication events, hybridization and regional selection. Our work has direct implications for mango breeding and genebank management, and also builds on recent efforts to understand how woody perennial crops respond to domestication. 1999; Matsuoka et al., 2002; Li et al., 2006; Londo et al., 2006; Introduction Huang et al., 2012; Hufford et al., 2013; Saintenac et al., 2013; Over the past 12 000 yr, humans have domesticated thousands of Von Wettberg et al., 2018) and, consequently, there remain species from across the plant kingdom (Meyer et al., 2012; Meyer many gaps in our understanding of the broader context of & Purugganan, 2013; Gaut et al., 2015). The process of crop domestication – across a wide span of taxonomic and geographi- domestication is a special case of co-evolution that gradually cal diversity, among species that have undergone different degrees increases plant–human interdependence, and results in various of domestication, and among species with different life-history levels of intensity of cultivation and breeding (Clement, 1999; strategies (Miller & Gross, 2011; Meyer et al., 2012). Zeder, 2006; Pickersgill, 2007). As such, the domestication pro- One of the central dogmas of domestication is that crops cess provides tractable systems in which to study convergent evo- undergo an often-severe decrease in genetic diversity in response lution, gene flow, adaptation, diversification and genome to three key bottleneck (or founder) events (Ladizinsky, 1985; evolution (e.g. Arnold, 2004; Kovach et al., 2007; Purugganan & Cooper et al., 2001; Doebley et al., 2006; Van de Wouw et al., Fuller, 2009; Meyer & Purugganan, 2013; Olsen & Wendel, 2010; Miller & Gross, 2011). During the initial stages of culti- 2013; The International Peach Genome Initiative, 2013; Wash- vation, as important traits are selected for or against, crops gen- burn et al., 2016). Understanding how these evolutionary forces erally undergo a ‘domestication bottleneck’ (Cooper et al., impact crop genetic diversity and characterizing the standing 2001; Van de Wouw et al., 2010). Compounding the primary genetic variation within cultivated germplasm is key to crop loss of diversity, many crops experience a secondary ‘dispersal improvement efforts (e.g. Iqbal et al., 2001; Burke et al., 2002; bottleneck’ when they are introduced into new geographical Esquinas-Alcazar, 2005; Doebley et al., 2006; Pickersgill, 2007; regions (Cooper et al., 2001; Van de Wouw et al., 2010). Soy- Gross & Olsen, 2010; Miller & Gross, 2011; Kassa et al., 2012). bean, for example, was subjected to an intense introduction bot- However, our current understanding of plant domestication is tleneck when it was introduced from Asia into North America founded on studies of highly domesticated annual staples like (Hyten et al., 2006). The concept of a dispersal bottleneck is cereals and grain legumes (e.g. Singh et al., 1991; Wang et al., connected to Vavilov’s premise of crop ‘centers of origin’, which Ó 2019 The Authors New Phytologist (2019) 222: 2023–2037 2023 New Phytologist Ó 2019 New Phytologist Trust www.newphytologist.com New 2024 Research Phytologist posits that the geographical origin of a crop contains the great- for more than a century, producing tons of fruit throughout their est variation of morphological types (Vavilov, 1987), thereby lifetime. implying a loss of diversity as a crop is dispersed. As breeding Most authors presuppose a single domestication event for cul- and cultivation intensify, some crops suffer a tertiary ‘improve- tivated M. indica (DeCandolle, 1884; Mukherjee, 1972; Vavilov, ment bottleneck’ (Cooper et al., 2001; Van de Wouw et al., 1987; Mukherjee & Litz, 2009; Singh, 2016), and on the basis of 2010). The drastic reductions in diversity incurred during these historical documents and artifacts, M. indica is thought to have three bottleneck events (primary, secondary, tertiary) can nega- been cultivated in India for thousands of years before it was intro- tively impact a crop’s ability to adapt to novel environments, duced elsewhere (Mukherjee, 1949; Fig. 1). Buddhist monks pests and diseases (e.g. Abbo et al., 2003; Esquinas-Alcazar, were likely the first to introduce mango outside its original range 2005). However, the relative impacts of each bottleneck vary of cultivation during their trips to Southeast Asia in the 4th and both within and among crops, depending in large part on the 5th centuries (Mukherjee, 1949). The mango began its westward biology of the species itself. journey much later, when Persian traders brought the tree to East Perennial crop species have recently received increased atten- Africa in the 9th or 10th centuries (Mukherjee, 1949). In the 16th tion highlighting their relatively different trajectories under Century, as global botanical trade continued to grow, the Por- domestication compared to annuals (Miller & Gross, 2011; Gaut tuguese likely reintroduced the mango into East Africa from their et al., 2015). In general, woody perennials retain greater levels of territory in Goa (Mukherjee, 1949). The Portuguese would con- genetic diversity under cultivation than do annual species (Miller tinue to facilitate mango’s range expansion, transporting it to & Gross, 2011). For example, recent genome-wide analyses of West Africa, and then to Brazil sometime around 1700 (Pope- peach (Prunus dulcis) and its close relative almond (Prunus noe, 1920; Mukherjee, 1949). From there, mango spread persica) showed no evidence of genetic bottlenecks associated with throughout the Caribbean, reaching Barbados in 1742 and domestication in either species (Velasco et al., 2016), and similar Jamaica by 1782 (Popenoe, 1920; Mukherjee, 1949). As a Span- results have been found for grape (Vitis vinifera; Myles et al., ish colony, Mexico had an unique history of introductions, with 2011) and apple (Malus x domestica; Gross et al., 2014). The rela- mangoes arriving from the Caribbean as well as directly from the tively weak primary domestication bottleneck observed in many Philippines, which also was under Spanish rule at the time (Pope- perennial species is largely a result of characteristics common to noe, 1920; Mukherjee, 1949). It was not until 1833 that the first the perennial life history: a long generation time and the predom- mango reached the shores of Florida (Popenoe, 1920). In the inance of self-incompatibility (Miller & Gross, 2011). The 1900s, mango became the subject of intensive breeding programs former means that perennial crops have experienced fewer gener- in South Florida, which produced many of today’s most impor- ations of selection under domestication than their annual coun- tant commercial cultivars including ‘Tommy Atkins’, ‘Haden’, terparts (Pickersgill, 2007), whereas the latter explains how ‘Keitt’ and ‘Kent’ (Knight et al., 2009). For this reason, South perennials maintain high levels of heterozygosity despite the fact Florida has been termed a secondary center of domestication for that their per-unit-of-time mutation rates are far slower than in mango (Knight & Schnell, 1994). annual species (Savolainen & Pyh€aj€arvi, 2007). In addition, Today, mango is one of the world’s most important fruits and clonal propagation techniques common in woody perennial culti- is grown in tropical and subtropical climates across the world – vation allow any individual including F1 hybrids, triploids and (FAO, 2003; FAOSTAT, 2018), with two primary cultivar types, sterile or seedless parthenocarpic individuals – to be preserved for Indian and Indochinese, being differentiated by a suite of mor- posterity, effectively halting the domestication process in that phological characters (Crane & Campbell, 1994). Indian culti- clone